AC-2020-12-1420.R1 – HIV care providers’ familiarity, concerns, and attitudes about HIV PrEP in Colombia: insights from the PrEP-Col-Study

ABSTRACT

In 2019, Colombia approved the combination of tenofovir disoproxil fumarate/emtricitabine for HIV Pre-Exposure Prophylaxis (PrEP). Therefore, we conducted a situational analysis in HIV-care providers to identify barriers and facilitators for PrEP implementation. A survey was applied to a non-probabilistic sample of health care workers of HIV-specialized clinics. We examined PrEP awareness and familiarity, comfort with PrEP-related activities, perceived barriers for PrEP implementation, concerns, and attitudes. Poisson regressions assessed the relationship between these factors and the variable “having a plan to offer PrEP”. The participation rate was 41% and included physicians (42.6%) and other health professionals (57.4%). Fifty-one percent of the participants reported more than five years of experience caring for people living with HIV. Forty-two percent of non-physician health care workers were nurses. Most reported high familiarity/comfort with PrEP-relevant activities. Concerns about PrEP were prevalent (> 50%) and included causing more harm than good, reducing condom use, medication non-adherence, drug resistance, and healthcare system barriers. Physicians had a plan to offer PrEP (72.2%) more often than other health professionals (52.6). Having a plan to offer PrEP was related to PrEP knowledge and comfort assessing sexual behavior and providing HIV counseling. Overall, about half of HIV-care providers seemed ready to offer PrEP and constitute an asset for PrEP implementation efforts in Colombia. PrEP awareness among non-physicians, PrEP concerns, and negative attitudes need to be addressed to enhance implementation.

KEYWORDS:

• Implementation science
• HIV Pre-Exposure Prophylaxis (PrEP)
• HIV prevention

Introduction

The incidence of HIV in Colombia continues to increase mainly affecting men who have sex with men (MSM), transgender women (TGW), and sex workers (SWs) (Montana et al., 2021; UNAIDS, 2018). HIV pre-exposure prophylaxis (PrEP) can reduce the risk of HIV acquisition by more than 90% in people at high risk and thus the World Health Organization (WHO) recommended its implementation and published evidence-based PrEP guidelines (Anderson et al., 2012; Fonner et al., 2016; OMS, 2017; ONUSIDA, 2015; Tan et al., 2017; WHO, 2015a, 2015b).

In January 2019, the Colombian medicinal drug regulatory agency (INVIMA) approved the combination of Tenofovir Disoproxil Fumarate and Emtricitabine (TDF/FTC) for use in “Patients at high risk for human immunodeficiency virus type 1 (HIV-1) infection, to reduce the probability of acquiring it, in addition to proper condom use and other protective measures”, (Minsalud, 2019) but PrEP has not yet been widely implemented. (OPS, 2019) PrEP implementation needs to be informed by the input from future users, health care providers, and health care organizations where the intervention is to be offered.

This article reports the findings in health care workers (HCW) from HIV care centers regarding their familiarity with, willingness to offer, skills related to, concerns about, and intention to offer PrEP and PrEP-related services.

Methods

Study design: We conducted a cross-sectional study in a non-probabilistic sample of HCW. This study was approved by the Institutional Ethics Committee for Human Research of the Corporacion de Lucha Contra el SIDA, Colombia (IRB 00005732, US DHHS; Approval Letter No. 053) and the Queen's University Health Sciences and Affiliated Hospitals Research Ethics Board.

Study population. We included all HCW working at HIV- specialized centers of the VIH-COL network who consented to participate. Potential participants were sent an e-mail invitation with a link to the online survey. A reminder message was e-mailed every fifteen days up to three times. A final reminder was sent by regular mail. We collected data between August and December 2019.

Measurements: We built a Qualtrics survey guided by the existing literature on PrEP (Sharma et al., 2014), previous surveys, and the Theoretical Domain Framework (TDF) model (Henderson et al., 2006; Huijg et al., 2014). The survey had 108 questions and could be completed in 30 min. For this report, we use demographic data, knowledge about and familiarity with PrEP, frequency and comfort with PrEP-related activities, PrEP training, experience with PEP, attitudes and concerns related to PrEP, and intentions to offer PrEP care (see details in Table S1, supplementary file).

Statistical analysis. First, we performed bivariate analysis to compare the covariates between two groups of HCW, physicians vs. non-physician HCW, and to evaluate the effect of the covariates and their relationship with the outcome. The outcome was “having a plan to offer PrEP care” (see details in Table S1). Prevalence ratios were estimated using a multivariate Poisson regression model with robust variance and constant exposure time equal to one (Barros & Hirakata, 2003; Coutinho et al., 2008). Covariates representing the same domain were summarized in an index variable and standardized through a percentage value scale from 0 to 100%. The handling of each covariate is detailed in Table S1). Data was recorded using Qualtrics with consistency checks. Stata / IC 16 was used for all analyses.

Results

Of 338 invited individuals, 140 (41%) subjects provided informed consent. From these, 129 (92.1%) answered more than 70% of the questions (Supplementary Figure). The average age of the participants was 37.5 ± 9.3 years. Most physicians were male (65%) while most non-physicians were female (79%). Half of the sample had five or more years of experience providing care to people living with HIV (PHA). Overall, participants were willing to care for people on PrEP (87.4%). However, non-physicians were less likely to have a plan (72.2% vs 52.6%) or to be willing to advocate for PrEP implementation (79.6% vs 54.4) (Table 1).

Table 1. General characteristics and intention to provide PrEP care in a sample of health care workers of Colombian HIV clinics.

	Physicians		Non Physicians		Total		P-Value
Age (average; SD)	39.4	9.9	36.1	8.6	37.5	9.3	0.0553
	n	%	n	%	n	%
Sex
Male	36	65.4	15	20.3	51	39.5	<0.001
Female	19	34.6	59	79.7	78	60.5
Years of HIV-related practice
Less than 5 years	19	37.3	40	56.3	59	48.4	0.029
5 - 10 years	13	25.5	19	26.8	32	26.2
More than 10 years	19	37.3	12	16.9	31	25.1
Health care discipline
HIV specialist	34	61.8	0	0	34	26.4
Infectious Disease specialist	6	10.9	0	0	6	4.6
General Physician	12	21.8	0	0	12	9.3
Specialist-(other than Infectious Disease specialist)	3	5.4	0	0	3	2.3
Nurse	0	0	31	41.9	31	24.0
Pharmacist	0	0	14	18.9	14	10.8
Social worker	0	0	9	12.2	9	6.9
Psychologist	0	0	16	21.6	16	12.4
Other	0	0	4	5.4	4	3.1
Job focus
“More than 90% of my time is dedicated to managing the clinic”	1	1.8	17	22.9	18	13.9	<0.001
“Most of my time dedicated to the care of patients”	45	81.8	32	43.2	77	59.7
“I have both, administrative and clinical work”	9	16.4	25	33.8	34	26.4
Intention: Extremely likely/very likely
Willing to provide PrEP-related care to patients	50	92.6	47	82.5	97	87.4	0.153
Has the intention to provide PrEP-related care	48	88.9	46	80.7	94	84.7	0.295
Has a plan to provide PrEP-related care	39	72.2	30	52.6	69	62.2	0.026
Would advocate for PrEP implementation in his/her organization	43	79.6	31	54.4	74	66.7	0.005

Overall, 85.3% of respondents knew about PrEP. Physicians reported higher levels of knowledge about PrEP than non-physicians in all the aspects inquired (See Table 2). About 57% of the participants reported having started a conversation about PrEP. Of these, a minority (19.4%) expressed enthusiasm when discussing this subject with others. Only 15 of 129 participants had managed PrEP patients in the last 12 months. Few physicians had received training on how to provide care to PrEP patients (28.3%) and in the use of instruments to determine PrEP eligibility. Only 14% of non-physicians had received training on PrEP-related counseling.

Table 2. Familiarity, skills, and experience with PrEP in health care workers from HIV clinics in Colombia.

	Physicians		Non-Physicians		Total		P-Value
Self-perceived knowledge on PrEP	n	%	n	%	n	%
Never heard about	1	1.8	4	5.4	5	3.9	<0.001
Very little knowledge	2	3.6	12	16.2	14	10.8
Some knowledge	8	14.6	38	51.3	46	35.7
Good PrEP knowledge	33	60.0	20	27.0	53	41.1
A lot of knowledge	11	20.0	0	0.0	11	8.5
Familiarity
How well do you know PrEP guidelines?	P50	RIC	P50	RIC	P50	RIC
CDC guidelines	4.0	1.2	2.0	1.8	3.0	2.4	<0.001
WHO PrEP guidelines	3.9	1.6	2.0	1.8	2.2	2.4	0.0001
Latin America PrEP guidelines	3.0	2.8	1.5	1.0	2.0	1.9	0.0014
Perceived knowledge of specific aspects of PrEP
PrEP efficacy on preventing HIV	4.4	1.0	3.0	2.0	4	1.5	0.0001
Frequency and severity of PrEP medications adverse effects	4.4	1.0	3.0	2.1	4	2.4	0.0001
Determining who could benefit from PrEP	4.6	1.0	4.0	1.8	4.1	1.9	0.0001
PrEP-related counseling	4.1	1.9	2.9	2.2	3.6	2.7	0.0001
Medications used for PrEP	5.0	0.7	3.8	2.4	4.1	2.0	0.0001
PrEP experience	n	%	n	%	n	%
Has anyone ever asked you about PrEP? Yes	47	87.0	39	68.4	86	77.5	0.019
Have you ever initiated a conversation about PrEP with one of your patients? Yes	38	70.4	25	43.9	63	56.8	0.005
Have you ever managed PrEP patients? Yes	9	16.4	6	8.1	15	11.6	0.157
When you talk about PrEP you feel …	n	%	n	%	n	%
Enthusiastic	21	38.2	4	5.4	25	19.4	<0.001
Neutral	14	25.4	18	24.3	32	24.8
Not enthusiastic	2	3.6	2	2.7	4	3.1
Anxious	1	1.8	1	1.3	2	1.6
No response	17	30.9	49	66.2	66	51.2
PrEP Training (Yes)	n	%	n	%	n	%
PrEP guidelines	22	41.5	5	8.8	27	24.6	<0.001
How to provide care to PrEP patients	15	28.3	5	8.8	20	18.2	0.012
PrEP-related counseling	14	25.9	8	14.0	22	19.8	0.154
Use of instrument to identify PrEP-eligible patients	9	16.9	2	3.5	11	10.0	0.025
Need more training (agree/completely agree)	45	83.3	56	98.2	101	91.0	0.007

P50: percentile 50; RIC: interquartile range.

Most participants frequently took a sexual history and felt comfortable doing so as well as assessing adherence to antiretroviral treatment, counseling patients, and monitoring drug therapy (Table 3). HIV testing was infrequent (the participants’ patients are mainly PHA), but 80% of physicians offered diagnostic tests for other sexually transmitted infections. Differences between physicians and non-physicians were observed for the frequency of some activities: offering HIV testing, informing about HIV diagnosis, and testing for sexually transmitted infections.

Table 3. Health care providers’ experience and comfort with PrEP-related activities in HIV clinics in Colombia.

	Physicians		Non-Physicians		Total		P-Value
Perception on the number of patients seen in the participant’s clinic from/to whom he/she … (proportion who reported “all or most of the patients”)	n	%	n	%	n	%
takes a sexual history	50	92.6	41	71.9	91	82.0	0.006
asks about risky or preventive behaviours	51	94.4	53	93.0	104	93.7	1.000
asks about sexual orientation	50	92.6	42	73.7	92	82.9	0.011
asks about their sexual partners’ HIV serostatus	48	88.9	46	80.7	94	84.7	0.295
counsels on HIV risk reduction	50	92.6	53	93.0	103	92.8	1.000
asks about gender identity	44	81.5	39	68.4	83	74.8	0.130
Frequency of activities (Every day-several times a week)
offering HIV testing	19	35.2	5	8.8	24	21.6	0.001
performing counseling on medication adherence	40	74.1	46	80.7	86	77.5	0.497
informing someone about a positive HIV test	13	24.1	18	31.6	31	27.9	0.405
asking patients about HIV medication adverse effects	42	77.8	41	71.9	83	74.8	0.518
performing HIV medication monitoring	41	75.9	34	59.7	75	67.6	0.073
offering diagnostic testing for sexually transmitted infections	43	79.6	7	12.3	50	45.0	<0.001
Comfort level (Totally comfortable-very comfortable)
asking patients about their sexual history	48	88.9	43	81.1	91	85.0	0.291
asking patients about their either risk or preventative behaviors	49	90.7	47	82.5	96	86.5	0.270
Asking the sexual orientation	44	81.5	44	81.5	88	81.5	1.000
asking about sex partners HIV serostatus	49	90.7	50	90.9	99	90.8	1.000
providing counsel on HIV risk reduction	52	96.3	53	93.0	105	94.6	0.679
asking about gender identity	45	83.3	43	81.1	88	82.2	0.805
offering HIV testing	50	94.3	44	95.7	94	95.0	1.000
counselling on HIV medication adherence	51	98.1	56	100.0	107	99.1	0.481
disclosing the HIV diagnosis to a patient	44	84.6	34	75.6	78	80.4	0.311
prescribing HIV medications	52	98.1	47	92.2	99	95.2	0.201
asking about HIV medication side effects	51	96.2	53	94.6	104	95.4	1.000
offering diagnostic tests for sexually transmitted diseases	54	100.0	36	83.7	90	92.8	0.003

Most participants were concerned that PrEP could do more harm than good if not implemented carefully, that it would lead to less condom use and anticipated problems with medication adherence. Besides, there were concerns that healthcare system barriers could hinder approval of medications, follow-up appointments, the inclusion of PrEP in prevention protocols, and the availability of time to provide PrEP services (Table 4).

Table 4. Health care workers negative attitudes, and concerns around PrEP in HIV clinics in Colombia.

Negative attitudes (completely agree/agree)	Physicians		No physicians			Total
	n	%	n	%	p-value	n	%
1.PrEP could cause more harm than good if not correctly implemented	33	64.7	50	71.4	0.431	83	68.6
2. PrEP will lead to decreased condom use	36	70.6	52	74.3	0.683	88	72.7
3. I believe it is unethical to prescribe HIV medications to healthy individuals	1	1.9	13	18.6	0.004	14	11.6
4. There are better alternatives for HIV prevention than PrEP	10	19.6	29	41.4	0.017	39	32.2
5. PrEP would not be better than current HIV prevention strategies	4	7.8	19	27.1	0.009	23	19.0
6. Few people in Colombia need PrEP	3	5.9	2	2.9	0.649	5	4.1
Concerns about adherence and drug resistance (A lot of concern)
1. Increased resistance to HIV medications	27	49.1	48	64.9	0.104	75	58.1
2. Lack of compliance with monitoring	46	83.6	62	83.8	1.00	108	83.7
3. Suboptimal medication adherence	47	85.4	58	78.4	0.365	105	81.4
4. Medication misuse, e.g., saling medications	50	90.9	61	82.4	0.205	111	86.1
Health system-related concerns (A lot of concern)
1.That the health care system does not approve PrEP medications.	41	74.6	47	64.4	0.251	88	68.7
2. Insufficient time to monitor and counsel people in PrEP	39	70.9	48	65.7	0.571	87	67.9
3.That the health care plans do not cover PrEP	37	67.3	47	64.4	0.851	84	65.6
4. That the health system does not allow to monitor people in PrEP.	41	74.6	53	72.6	0.842	94	73.4

Having a plan to care for people on PrEP was more common among physicians, among those who were knowledgeable about PrEP, knew PrEP management guidelines, frequently assessed sexual behaviors, and provided counseling (Table 5). Having received training in and having experience with PrEP were not related to having a plan. Those who said they needed more PrEP training were less likely to have a plan. Neither the attitudes nor the concerns were related to having a plan.

Table 5. Univariate Poisson regression analysis of the factors associated with having a plan to manage people on PrEP in health care workers of Colombian HIV clinics

Variables	Prevalence ratio	[Conf. Int-95%]		P-value
Age(quartile)
≤ 29 years	reference
30–37 years	1.428	0.929	2.195	0.104
38–43 years	1.250	0.777	2.011	0.358
>43 years	1.273	0.788	2.056	0.324
Sex (Male)	1.335	1.001	1.781	0.049
HCW (Physicians vs non-physicians)	1.372	1.018	1.849	0.037
Familiarity with PrEP
Self-perceived knowledge about PrEP (some knowledge + a lot of knowledge vs others)	1.371	1.013	1.854	0.041
Knows any of the PrEP guidelines (yes vs no)	1.376	1.035	1.829	0.028
Knows clinical aspects of PrEP (scale from 5 to 25)	1.016	0.987	1.044	0.278
PrEP-related training
Having ever received PrEP training, Yes vs no	1.307	0.980	1.742	0.068
Need more training (agree/completely agree vs other categories)	0.647	0.497	0.843	0.001
Experience with PEP - (at least once a month vs other categories)	0.868	0.512	1.473	0.601
Experience in clinical activities related to PrEP
Number of people in whom PrEP-relevant activities are performed (scale from 9 to 30)	1.055	1.009	1.103	0.018
Frequency of the activity (scale from 6 to 42)	1.013	0.996	1.029	0.133
Comfort level
Level of comfort(scale from 22 to 60)	1.018	0.998	1.040	0.083
PrEP-attitudes and related concerns
Level of agreement with negative attitudes (scale from 2 to 22)	0.986	0.944	1.029	0.514
Level of concern on medication use (scale from 8 to 20)	1.016	0.962	1.073	0.569
Level of concerns on health system barriers (scale from 4 to 24)	0.992	0.949	1.036	0.708

Discussion

This study is the first in Colombia to generate evidence on HCW’s factors that can impact PrEP implementation. HCW in this sample possess attributes that can support PrEP implementation in the clinics where they practice: They were experienced in the use of antiretroviral drugs, knew the concept of PrEP, have discussed PrEP with their patients, felt comfortable obtaining a sexual history and assessing risk behaviors, and often ordered diagnostic tests for sexually transmitted infections. Almost all the physicians in this sample were aware of PrEP and 80% of them reported having substantial PrEP knowledge. Yet, an important proportion of physicians (20%) and most non-physicians would benefit from further PrEP education to enhance adoption. A systematic review of 28 studies found that healthcare providers reported insufficient knowledge on PrEP leading to discomfort in prescribing and insufficient levels of PrEP provision (Pleuhs et al., 2020). Interestingly, while the willingness in the whole sample to provide PrEP was high (87.4%) and having a plan was relatively high (62.2%), only 38% of physicians and 5.4% of non-physicians were enthusiastic when talking about PrEP. This contrast could be related to concerns about prescribing PrEP reported by participants: the possibility of medication misuse, reduction of condom use by PrEP users, health system barriers, and the perceived lack of autonomy to start PrEP. These concerns are consistent with studies in the United States and Europe that identified similar factors as barriers to PrEP prescription, among which the cost of drugs was the most prominent. (Desai et al., 2016; Di Biagio et al., 2017; Hayes et al., 2019; Krakower et al., 2014; Plomer et al., 2020; Sanchez-Rubio Ferrandez et al.2016). These findings highlight the need for PrEP education with special attention to concerns and misperceptions.

Although experience with PrEP in this sample was low (16.4% of physicians had any previous PrEP experience), by 2019, physicians were prescribing PrEP in Colombia suggesting that capacity already existed and could be escalated. Reasons for the limited experience in PrEP include that TDF/FTC is not covered by the Colombian public health benefit plan, there are no Colombian PrEP guidelines, and PrEP is not widely advertised. Despite this, most participants (physicians and non-physicians) acknowledged having had discussions with other individuals about PrEP.

The WHO recommends that PrEP programs could be integrated into services already provided to key populations since clinics offering these services often have the infrastructure and human capacity to initiate a PrEP service (OMS, 2017). Our results suggest that most of the elements necessary for PrEP adoption are already in place in the participating institutions (clinics of the VIH-COL network).

Strengths and Limitations.

This study gathers perceptions from HCW of different disciplines, both physicians and non-physicians, all of whom would eventually contribute to PrEP delivery. The response rate (41%) in this study is higher than in other surveys elsewhere whose response rate ranged from uncalculated (likely very low)(Reyniers et al., 2018; Sharma et al., 2014; Sinno et al., 2021) to around 10%. (Blackstock et al., 2017; Cimen et al., 2020; Desai et al., 2016). Notably, by 2019, the VIH-COL network served approximately 24,000 PHA, a sizable proportion of the 115,000 PHA on treatment in Colombia. Yet, we may have overestimated PrEP awareness, willingness and plans since two clinics were participating in a PrEP demonstration study. This sample may not represent other HIV-specialized clinics and surely does not represent primary care HCW. Our small sample also precludes comparisons between the disciplines pooled under the non-physician category.

Conclusions

HIV-specialized clinics in Colombia represent an asset for early national PrEP implementation, but still need PrEP education focused on facilitating the adjustment of existing skills to PrEP delivery and correcting misperceptions linked to negative attitudes. It is essential that the health system barriers, specifically medication coverage and physicians’ lack of autonomy to offer PrEP, be overcome via a government-supported HIV elimination program.

Authorship: JMC designed the study, interpreted analysis, and wrote the manuscript; BAL designed the study and assisted with study conduction and statistical analyses; HMM collected the survey data, performed the statistical analyses, and critically revised the manuscript; EMB, JTI, MA, PC, and XGO critically revised the manuscript.

Declaration of conflict of interests

The authors declare that there is no conflict of interest.

Acknowledgments

We thank the VIHCOL network for assisting in the recruitment of survey participants.

Disclosure statement

No potential conflict of interest was reported by the author(s).

Additional information

Funding

This work was supported by grants from the Ministry of Science-Colombia (code: 334780762872).